Three-Dimensional Sonography in Diagnosis of Retroperitoneal Hemorrhage From Adrenocortical Carcinoma
Rafal Z. Slapa, MD, Anna A. Kasperlik-Zaluska, MD, Jerzy A. Polanski, MD, Krystyna Borowicz, MD, Malgorzata Serafin-Krol, MD, Wieslaw Jakubowski, MD
Abbreviations
CT, computed tomography; MPR, multiplanar reforma- tion; 3D, 3-dimensional; 2D, 2-dimensional
Received May 10, 2004, from the Department of Diagnostic Imaging (R.Z.S., M.S .- K., W.J.) and Second Department of Surgery (J.A.P.), Medical Faculty II, Medical University of Warsaw, Warsaw, Poland; Department of Endocrinology, Center for Postgraduate Medical Education, Warsaw, Poland (A.A.K .- Z.); and Department of Pathomorphology, Czerniakowski Hospital, Warsaw, Poland (K.B.). Revision requested May 18, 2004. Revised manuscript accepted for publi- cation June 14, 2004.
This study was supported by State Committee for Scientific Research (Komitet Badań Naukowych) grant 6 P05B 072 20.
Address correspondence and reprint requests to Rafal Z. Slapa, MD, Department of Diagnostic Imaging, Medical Faculty II, Medical University of Warsaw, ulica Kondratowicza 8, 03-242 Warsaw, Poland. E-mail: r.slapa@acn.waw.pl.
S onography has limited value in visualization and differen- tiation of adrenal masses, although sonography of the abdomen can usually show adrenal tumors with a maxi- mal diameter of greater than 1 cm on the right side and 1.5 to 2 cm on the left side.1 Small tumors often have a homoge- neous echo texture that becomes heterogeneous as the tumor grows.2 Central necrosis or hemorrhage within the tumor may result in a hypoechoic area.3 Sonography is useful for follow-up of nonhyperfunctioning adrenal masses diagnosed on the basis of computed tomography (CT) or magnetic resonance imaging as adenomas.4 Sonography is the method of choice for the visu- alization of adrenal masses in small children.5,6 Diagnosis of adrenal masses in pregnant women can be established only with noninvasive methods such as sonography or magnetic res- onance imaging.7
Three-dimensional sonography has been recognized and studied for 20 years.8 However, only recently, because of developments in computer techniques and in the construction of scanners, has the acquisition of volumes with automatic 3-dimensional (3D) probes become more simple and the quality of the images acquired in 3D sonography improved to compare with conventional sonographic images. With the matrix or automatic 3D probes and fast com- puters now available, even real-time 3D sonography (4-dimen- sional sonography) has become possible.
In 3D sonography, the volume of tissues can be analyzed inter- actively in 3 perpendicular planes in the multiplanar reformation (MPR) mode or as a rendered image of the 3D object on a plane through the application of various algorithms. From 2001 through 2003, we investigated the application of 3D sonography for the evaluation of adrenal masses. The purpose of the proce- dure was explained to the patients, and their informed consent was obtained.
Here we report the diagnosis of retroperitoneal hemorrhage from adrenal carcinoma on the basis of 3D sonography.
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Case Report
A 22-year-old woman was admitted with signs of acute appendicitis. In the sonographic examina- tion performed at admission, a right adrenal region tumor measuring 70 x 41 × 50 mm was detected. At the lower pole of the tumor, close to the kidney, a solid additional lesion of 22 mm in diameter was noted. The enlarged paracaval lymph node was visualized. Examination of the specimen after appendectomy disclosed signs of inflammation.
After the appendectomy, contrast-enhanced CT examination showed a nonhomogeneous tumor of the right adrenal gland and enlarged paracaval lymph nodes (Figure 1). The tumor had partly irregular margins at the lower pole, which could have indicated local invasion by the tumor. The fatty capsule around the entire right kidney, enclosed by the fascia of Gerota, had increased density (Figure 2).
An endocrinology consultation revealed no clin- ical signs of adrenal hyperfunction, and blood tests revealed a mildly elevated androstenedione level, a cortisol level close to the upper limit, and a normal dehydroepiandrosterone sulfate level. Urine culture results were negative.
One day after the onset of acute right flank pain and 3 weeks after the initial conventional sonographic examination, 3D sonography was performed with a dedicated 4-dimensional
sonographic scanner (Voluson 730; GE Medical Systems, Kretz Ultrasound, Zipf, Austria) equipped with an automatic convex 2- to 5-MHz 3D probe. The examination revealed a heteroge- nous adrenal gland tumor measuring 75 x 62 × 90 mm. The mass had a hypoechoic, partly subcap- sular area of hemorrhage extending to the lower pole of the tumor. The hypoechoic region (50 x 40 x 30 mm) in the continuation of the intratumoral hemorrhage was localized at the upper pole of the kidney, close to the renal artery, and represented the retroperitoneal hemorrhage. With the use of the unique imaging capability of 3D sonography, the continuity of the hemorrhage was evident in the plane parallel to the ultrasonic probe (Figure 3). The 2-dimensional (2D) and 3D power Doppler examinations revealed only a few vessels inside the tumor plus the dominant lower adrenal artery. The right adrenal vein going to the inferior vena cava was seen only on 3D power Doppler sonography (Figures 4-6). The supplying vessels had a distribution pattern characteristic of adrenal tumors. Three-dimensional power Doppler sonography visualized the neighboring vessels. The main renal artery and the separate branch to the upper pole were also seen close to the retroperitoneal hemorrhage. Enlarged para- caval lymph nodes were observed. No other sites of tumor were visualized in the abdomen.
A tumorectomy with an adrenalectomy was performed. The surgery revealed the retroperi- toneal tumor with a gelatinous focus of hemor-
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rhage at the upper pole of the kidney. Close to the level of the retroperitoneal hemorrhage, there were 2 renal arteries, the main and the branch to the upper pole. Some of the enlarged paracaval lymph nodes were removed.
On macroscopic examination, the tumor mea- sured 100 × 90 × 60 mm with foci of necrosis and laceration of the capsule. Microscopic examination disclosed adrenal carcinoma with hemorrhagic and necrotic areas constituting 50% of the tumor. In the paracaval lymph nodes, metastases were observed, and in the neighboring retroperitoneal fatty tissue, malignant infiltrations were found.
Postsurgery bone scintigraphy did not identify any metastatic changes. The androstenedione level remained increased. The patient was treated with antibiotics, hydrocortisone, and mitotane and subsequently with chemotherapy. After the first cycle of chemotherapy, there were many neo- plastic masses in the retroperitoneum. The patient did not come for the next cycle of chemotherapy and died 6 months after the right adrenalectomy.
Discussion
Adrenocortical carcinomas are rare adrenal mass- es in that they constitute only between 0.05% and 0.2% of all cancers. This translates to a rate of only 2 cases per 1 million in the world population.9 Adrenocortical carcinomas are usually large and highly aggressive tumors with local invasion and distant metastases, which can be found even with small tumors.10 They contain areas of hemorrhage and necrosis of variable degrees.11 A retroperi- toneal hemorrhage can be one complication of this very friable tumor.3,12
In the records of the Department of Endo- crinology of the Center for Postgraduate Medical Education (Warsaw, Poland), among 137 adrenal carcinomas studied, there were just 2 cases of retroperitoneal hemorrhage (A.A.K .- Z., unpub- lished communication). In both cases, retroperi- toneal hemorrhage was the first symptom of an adrenal tumor and was a life-threatening event, which, because of massive hemorrhage, necessi- tated treatment by surgery with resection of the tumoral masses. In both cases, local infiltration and metastases to the lungs appeared quickly after the adrenalectomy. A primary adrenal cyst or tumor was reported to be the fourth most common cause of spontaneous retroperitoneal hemorrhage after renal cell carcinoma, angio- myolipoma, and renal artery aneurysm.13
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Patients with an adrenal carcinoma may pre- sent with local flank pain, symptoms related to metastases or as a manifestation of unregulated hormone production by the tumor. The term functioning tumor is used to refer to a tumor that produces an unregulated, excess amount of hor- mone, which results in clinically detectable signs.
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A nonfunctioning tumor may produce 1 or more hormones, but they are present in normal quan- tities or are not sufficiently differentiated to pro- voke clinical manifestations.3 Nonfunctioning adrenal carcinomas may be found incidentally.14
In this case, the adrenal carcinoma was an inci- dental finding on abdominal sonography per- formed before an appendectomy. In the initial sonographic examination, the lesion that proved later to be a hemorrhage had a solid appearance, which is typical for an early stage hematoma.12
On contrast-enhanced CT, the carcinoma was unevenly enhanced, indicating regressive changes inside the tumor. The retroperitoneal hemor- rhage could hardly be visualized because of the increased density of the fatty capsule around the kidney, similar to the density of the tumor, which could have indicated local invasion by the tumor. Opacification of the perirenal fat around the entire kidney was an indirect sign of hemorrhage and resulted from edema due to an inflammato- ry process or dissemination.
Three weeks later, during 3D sonography, how- ever, the retroperitoneal hemorrhage had high contrast to the tumoral tissue. A thorough evalu- ation of the gray scale images in planes parallel to the ultrasonic probe showed that the lesion out- side the adrenal mass was contiguous with the intratumoral hemorrhage. This finding con- firmed the speculative diagnosis made on the basis of evaluation of classic sonographic planes. Careful interactive evaluation of the acquired volume in the multiplanar mode seems particu- larly useful in complex anatomic situations.
Three-dimensional power Doppler sonography was also better than 2D power Doppler examina- tion in the visualization and identification of ves- sels supplying the tumor. During interactive evaluation of 3D power Doppler sonography, there are not the time constraints that are typical for abdominal 2D sonography, and adrenal ves- sels can be traced to their junctions with main vessels with high spatial precision in the MPR mode. Volume rendering permits high-resolu- tion vascular images resembling radiologic angiographic studies to be obtained.
The arterial supply to the adrenal glands comes from 3 major feeding vessels. The superior adrenal artery arises from the inferior phrenic artery; the middle adrenal artery comes directly from the aorta; and the inferior adrenal artery is a branch of the renal artery. These main arterial trunks do not input directly into the adrenal
gland but give off numerous small branches that resemble the teeth of a comb as they arise from the major adrenal arteries. Unlike the arterial supply, there is a single vein draining each gland. On the right side, the adrenal vein inputs direct- ly into the inferior vena cava. On the left side, the adrenal vein joins the inferior phrenic vein before emptying into the left renal vein.3
Three-dimensional power Doppler visualiza- tion and identification of feeding and draining vessels of large tumors, with a characteristic adrenal distribution, may permit diagnosis of adrenal tumors that infiltrate or displace adja- cent organs and whose origin may not be evi- dent on high-resolution cross-sectional studies. Visualization of the supplying vessels may be possible even in hypovascular large adrenal tumors.
Retroperitoneal hemorrhage may be a life- threatening event leading to serious hypovolemia. Moreover, the diagnosis of retroperitoneal hemor- rhage from adrenocortical carcinoma is a poor prognostic factor that can lead to quick dissemi- nation of the cancer and death. Three-dimension- al sonography may be more precise than CT in delineation of the extent of retroperitoneal hem- orrhage from adrenocortical carcinoma and can be a valuable diagnostic tool.
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